Abstract
Compared to urban residents, rural populations are less likely to engage in colorectal cancer (CRC) screening. As part of a statewide cancer needs assessment, we aimed to elicit rural perspectives about CRC screening and resources. We conducted three focus groups with rural Nebraska cancer survivors and caregivers (N = 20) in Spring 2021 using a collective case study design. Participant awareness of and knowledge about CRC screening methods varied across focus groups; overall, 95% of participants had heard of colonoscopy. Participants were less familiar with fecal tests and had confusion about them. Colonoscopy was associated with negative perceptions regarding the time, cost, and discomfort of the preparation and procedure, but some providers did not discuss alternative methods unless the patient resisted colonoscopy. Healthcare providers played a key role educating rural communities about CRC screening recommendations (age, risk) and testing options and being persistent in those recommendations. CRC awareness campaigns should include a variety of communication channels (TV, radio, billboards, health fairs, churches, healthcare settings). Promotion of CRC screening should include education about screening age guidelines, alternative test types, and informed decision-making between provider and patient regarding preferred screening methods based on the pros and cons of each test type. Individuals with a family history of colon issues (Crohn’s disease, CRC) are considered high risk and need to be aware that screening should be discussed at earlier ages.
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Introduction
Cancer services are underused by rural residents in the United States (US) [1]. Rural residents often need to travel long distances to obtain cancer screening, diagnostic services, and treatment, and weather-associated road conditions and lack of public transportation may further impede care [2]. Additionally, healthcare accessibility, especially specialized cancer care, is aggravated by low socioeconomic status and lack of health insurance [1]. Such accessibility issues are associated with adverse cancer outcomes for rural compared to urban residents, including later stage of diagnosis and higher mortality rates [1] and poorer quality of life [3]. A US cancer registry study showed that incidence rates of cervical, lung, and colorectal cancer (CRC) were significantly higher among rural residents [4]. Furthermore, a study of Medicare recipients found that rural versus urban cancer patients had worse health-related qualify of life including poorer vitality for CRC patients [3].
CRC is a major health concern in the US, with approximately 150,000 people newly diagnosed and 50,000 deaths in 2021. It is ranked third among cancers for new diagnoses and second leading cause of deaths [5]. CRC screening measures can reduce the incidence of CRC by identifying (and removing during endoscopy exams) pre-cancerous polyps. Screening can also identify cancer in earlier stages when it is more treatable and individuals have better survival rates. Therefore, screening plays an important role in state and national cancer prevention and control efforts.
In May 2021, the US Preventive Services Task Force (USPSTF) released the final CRC screening recommendation statement, extending recommended screening to ages 45–49 for those at normal risk and maintaining screening recommendations for ages 50–75. Screening for age 76–85 is not generally recommended but may be determined on a case-by-case basis. The recommended screening intervals depend on the screening method: high sensitivity guaiac fecal occult blood tests (HSg FOBT) or fecal immunochemical test (FIT) every year, stool DNA-FIT every 1 to 3 years, computed tomography (CT) colonography every 5 years, flexible sigmoidoscopy every 5 years, flexible sigmoidoscopy every 10 years plus annual FIT, or colonoscopy every 10 years [6].
Odds of CRC screening are lower for rural vs. urban residents [7]. In Nebraska, rural primary care patients were less likely to be up-to-date on CRC screening than their urban counterparts (74.4% vs. 88.1%) and colonoscopy use in the past 10 years was significantly lower among rural patients (71.9% vs. 87.5%) [8]. However, rural–urban difference in the use of FOBT was not statistically significant (rural: 12.4%; urban: 7.5%) [8]. Moreover, results showed several misconceptions are present regarding CRC screening: a lower proportion of rural patients stated that they can prevent themselves from getting CRC (41.3% vs. 55.8%); they would live no longer than 5 years with CRC (8.2% vs. 15.5%); and CRC screening costs too much (34.7% vs. 18.0%) [8].
As part of a statewide cancer needs assessment, team members at the University of Nebraska Medical Center (UNMC) collaborated with the Nebraska Comprehensive Cancer Control Program (NECCCP), Nebraska Cancer Coalition (NC2), and four rural cancer centers to conduct focus groups with cancer survivors and caregivers to learn about CRC screening. A person is considered a cancer survivor from the time of diagnosis, regardless of whether the person is actively receiving treatment, so we used the terms patient and survivor somewhat interchangeably. Because survivorship care is an integral component of cancer care, often with increased contact with the health care profession for continued monitoring of cancer status, treatment, and long-term side effects, we were interested in learning more about cancer survivors’ and caregivers’ experiences and perceptions about CRC screening. We assumed that this population of cancer survivors and caregivers might be better informed than the general population on the topic. Prior focus group studies have focused on cost, fears, attitudes, and beliefs associated with CRC screening [9, 10]. Our questions were as a follows: (1) What factors impact CRC screening in rural communities? and (2) What are suggested strategies to improve CRC screening in rural communities?
Methods
The UNMC Institutional Review Board deemed this qualitative collective case study [11] non-human subjects research as part of an institutional needs assessment. Prior to the beginning of each focus group, the purpose of the group was reviewed along with how information would be shared and the rationale for recording the session.
Team
The female assessment team consisted of cancer epidemiologists (KLR, SWG), a qualitative researcher (DD), public health students (JR, KN), a community outreach program coordinator (LBL), and cancer program administrators (TR, LS). Three members were present at each focus group filling the roles of facilitator (KLR), polling (JR, LBL), and notetaker (SWG, LBL, KN). Prior to initiating data collection, we held two practice sessions with public health students.
Setting
Cancer centers were located in central and western Nebraska counties classified 3–5 on the Rural–Urban Continuum Code, in cities with populations ranging from 25,000 to 51,000 and serving small outlying communities. Data collection occurred between February and May 2021. All focus groups were held virtually due to COVID-19 restrictions.
Recruitment and Eligibility
Cancer center staff distributed recruitment flyers at clinic appointments and support groups and posted copies in lobbies. The flyer stated the study purpose, topics, eligibility criteria (30 years and older, cancer patient/survivor or cancer caregiver, and Nebraska resident), and compensation ($40 gift card). Age 30 is outside the screening guidelines but encompass adults who may be caring for aging family members. The flyer contained assessment team contact information; later versions also had a QR code and web address for a screening survey administered through REDCap (Research Electronic Data Capture). The survey included age and residence screening questions to confirm eligibility and collected name, contact information, and general availability for the focus group. A team member contacted potential participants who had completed the survey to schedule the focus groups and to offer Zoom tutorials for any who were unfamiliar with the technology.
Procedure
Zoom is a cloud-based video conferencing platform accessible via computer or a free app. It also allows phone call-in. Zoom enables pre-built polling questions with point-and-click response. Sessions lasted 75 to 90 min and had 6–8 participants per group. Sessions were audio and video recorded and included built-in poll questions. In two instances, a survivor/caregiver dyad participated using one device. In those situations, poll responses were electronically captured for one participant and verbally reported for the other. Participants were instructed to keep their cameras on throughout the session. At the conclusion, participants were encouraged to contact the team if they had any questions or concerns. Gift cards were mailed within 2 weeks of the session.
Facilitation Guide
Team members (KLR, SWG, JR) and NECCP set the scope and general content of the facilitation guide, which was then modeled on a health needs assessment [12], with editing input solicited from the participating cancer centers. The guide attempted to balance participant engagement with time constraints. It was divided into two main sections plus a short conclusion: (1) general cancer experiences (general community health status, cancer diagnosis and treatment, and sources of cancer-related information) which is reported elsewhere [13] and (2) CRC screening (Online Resource 1). The guide included open-ended discussion questions, prompts, and probes with some marked as “time permitting.”
Coding and Analysis
A professional transcription service created verbatim transcripts from the audio recordings, which were reviewed by the team for accuracy. Analysis was based on a directed content analysis approach [14] with several processes implemented to ensure data validity and trustworthiness [15]. We maintained Word documents (transcripts, annotations, codebook, meeting notes) with editing software (track changes, comments) saved to a shared file repository that tracks document edits to serve as an audit trail for dependability and confirmability. SWG deductively developed broad initial codes from the guide and reviewed them with KLR. They served as primary reviewers and independently handled initial coding and analysis, inductively adding subthemes and reconciling differences across multiple rounds of review to develop a codebook, which was used for analysis of remaining transcripts. Subthemes were added when content did not fit into existing codes to ensure data saturation. Triangulation was achieved via regular check-in with the extended team for credibility and to ensure alignment. Thick description was used to contextualize the findings for transferability.
Results
Seven of the 27 people who completed the screening did not participate, including a physician testing the registration process before sharing flyers with patients, three individuals who were unresponsive to multiple contact attempts, one with a scheduling conflict, and two no-shows. Of the 20 participants, most (n = 16) self-identified as survivors, one of whom reported dual roles (survivor and caregiver), and the remaining 4 were caregivers. Two sessions included spousal dyads in which one spouse cared for the other. In such cases, the type of cancer was reported only for the survivor. Participants indicated the following cancer diagnoses: bladder, breast, lung, lymphoma, multiple myeloma, and prostate (Table 1).
Participants had many thoughts about factors impacting CRC screening. Most focused on negative aspects or barriers, although some also identified factors that promote screening. These factors were grouped into the following themes: information and awareness, role of healthcare providers, perception and attitude, and test-specific factors (Table 2). Participants also provided suggestions to improve messaging and CRC screening uptake. Based on the poll results and participant discussion, health education about CRC varied geographically in terms of testing types and level of awareness (Fig. 1).
Information and Awareness
Information and awareness primarily centered on screening knowledge—guidelines, tests, and sources of information about CRC and CRC screening. Some participants had a general lack of awareness about CRC, indicating that “it’s something that nobody likes to talk about,” although many participants knew someone who had CRC, including family and community members. Discussion also revealed misinformation about CRC, reflecting a misunderstanding of risk factors and the relationship between CRC and other types of cancer.
Knowledge of Screening Guidelines
Although a few participants knew CRC screening should begin at age 50, most did not. They reported a general lack of knowledge about screening guidelines. One participant thought rural areas may have more people who lack awareness of the need for CRC screening. Multiple participants made unfavorable comparisons between CRC and breast cancer screening awareness, with comments such as “You don’t hear about that you should. It’s not…[like] mammograms.” Interestingly, participants with a family history of colon problems (CRC, Crohn’s disease) were more familiar with CRC and colonoscopy but some were still misinformed. For example, a male survivor in his 30 s indicated that he had a family history of CRC and said it’s “probably something in…future to get screened for” but he was unaware that he should begin screening before the general age guidelines due to his family history risk. In contrast, others with a family history were more knowledgeable and made sure to get screened.
Knowledge of Screening Tests
Based on polling, only one participant was unfamiliar with any type of CRC screening test. All others knew about colonoscopies. Several participants expressed unfamiliarity with options other than a colonoscopy, and there was confusion about fecal tests. Multiple participants specifically mentioned Cologuard, which is the only Food and Drug Administration-approved stool DNA screening test for CRC currently available in the US market. Despite name recognition, they did not know how to classify Cologuard for the poll. They knew it was an at-home stool test but did not identify it with DNA testing. Thus, the poll results reflected misclassification as FOBT or FIT. Participants were also uncertain about the accuracy of stool-based tests, although one older male started using Cologuard after he heard it was highly accurate.
Sources of Screening Information
Participants primarily received information about CRC screening from primary care physicians (PCP) and their local cancer center. Others worked in healthcare settings and received information about screening tests at work. In addition to TV ads, some participants had heard TV celebrities such as Al Roker talk about CRC during CRC Awareness Month. Others did not know there was a month dedicated to CRC awareness and suggested creating one to promote awareness.
Role of healthcare providers
Healthcare providers appeared to play a key role in educating rural communities (and more specifically their patients) about CRC screening in terms of recommending screening and educating about screening options.
Recommending Screening
Some participants believed that older adults may be more aware of CRC (compared to younger people) because healthcare providers tell them to get screened. Several participants indicated that they wait to be told that a screening is needed. Specifically, they mentioned a PCP recommending cancer screening or reminding when (how often) to do it. Other participants pointed out that PCPs are not consistent about recommending screening. One survivor older than age 75 had a colonoscopy at age 55 and “it really wasn’t brought up much after that.” He expressed gratitude that he was now old enough to no longer need to worry about it. Participants thought younger (versus older) doctors were more likely to focus on preventative care and were more likely to recommend cancer screening in general. A caregiver described how she insisted her mother get a colonoscopy, but the mother “didn’t think it was necessary” because the PCP never recommended it. Participants felt the persistence and insistence of the PCP also impacted CRC screening. Participants used words such as “insist,” “harping,” and “harassed” to describe the PCP’s approaches to pushing patients to get a colonoscopy.
Educating About Screening Options
Several participants reported that colonoscopy is the recommended screening method, and discussions about alternative screening methods did not occur until they expressed hesitancy about colonoscopy. One older male indicated that for his first CRC screening, his PCP “just recommended to get [colonoscopy]. If there were other options, the doctor didn’t mention any.” When it was time to repeat the screening, “I didn’t want to do another colonoscopy.” He had seen TV ads for Cologuard, so he asked about that and “we went that route instead.” Likewise, a caregiver reported that her mother refused to get a colonoscopy, and only then did the PCP mention the alternative, non-invasive fecal test, which the mother agreed to do.
Perception and Attitude
The general opinion was that CRC is perceived as an “old person disease” and more particularly “an old man disease” with low perceived personal risk. “I’ll get [screened] later.” However, one participant pointed out that such attitudes lead to situations in which “when they find out, then it’s fatal.” An older male cited both generational and gendered attitudes characterized by “Mom said walk it off” in which health problems do not need to be addressed unless they are causing severe distress, particularly among males who have an “I’m fine” attitude. He felt such an attitude meant older people were less likely to be screened. Additionally, CRC was “something that nobody likes to talk about” and is often the subject for embarrassment and jokes, particularly related to colonoscopies.
Test-specific Factors
Colonoscopy
Although nearly all participants had heard of a colonoscopy, they did not have positive comments about it. Several participants said people were scared of the colonoscopy preparation and procedure, describing the bowel prep as “unpleasant,” “uncomfortable,” “inconvenient,” and time consuming. Additionally, sexual connotation and embarrassment of the procedure make people reluctant to undergo screening. The procedure is invasive, requires patients to go to the hospital, and is costly. An older male survivor noted, “there are a lot of people who financially can’t afford it. Even with insurance, your copays, you can go in and come out with a pretty hefty bill.”
Fecal Tests
In comparison, fecal tests such as Cologuard were perceived as convenient, easy, and private. One survivor commented that he decided to use Cologuard when he found out that it was 90% effective.
Suggestions to Improve CRC Screening
Participant suggestions to improve CRC screening focused on increasing awareness (dissemination methods), messaging suggestions, and addressing general community needs.
Increasing Awareness
Participants disagreed about methods of educating the public. Several people suggested that CRC outreach should follow other clinic-based education campaigns (e.g., prenatal/childbirth information, breast cancer awareness of mammograms, diabetic education) with posters and brochures in the clinic waiting and exam rooms. Others did not think those methods would be effective. Another suggestion was to incorporate CRC awareness into a local health education outreach method used by one of the cancer centers called “Stall Stories” in which laminated educational materials are posted in healthcare restroom facilities. They suggested using church groups, having a presentation with the monthly senior citizen informational dinners in which guest speakers present on different topics, and getting the community’s Relay for Life back. A participant suggested that the Relay for Life mini-health fairs provided opportunities for in-person contact with someone who had personal experience with CRC, which would be an effective method of increasing awareness. Other suggestions included using media preferred by the target age group (a “radio blitz”), billboards, and targeted media during CRC awareness month.
Messaging
Ideas for messaging included the need to convey that CRC is not a joking matter and to remove the sexual connotations from CRC and colonoscopy. However, participants did not have concrete ideas about how to accomplish this. One participant suggested using birthday reminders about getting screened such as “Give yourself a birthday present so that you have time for family and grandkids.” Participants cited the need for general education about CRC and the screening guidelines, so patients do not rely solely on doctors to tell them when to be screened. Other messages included a focus on letting the community know newer bowel preparation medications are more tolerable, and that there are alternative tests available (Cologuard).
General Community Needs
Participants were sensitive to cultural diversity factors related to accessing primary health care and cancer screening. They identified the need for better primary care for minority populations, specifically the Latinx population but extending to the wide diversity of cultures in their community associated with the meat packing industry. They noted the difficulty in providing culturally and linguistically tailored healthcare and suggested recruiting more bilingual PCPs and offering free or low-cost primary care clinics, even if only available once or twice a year, modeled on dental clinic outreach in the area. Financial assistance was also mentioned. Such actions, they believed, would improve the basic health needs in the community and increase preventative care, including CRC screening. The general public needed more education about cancer screening guidelines (ages, tests) because some people do not see a physician regularly and therefore are not told to be screened.
Discussion
Our focus groups conducted with rural Nebraska cancer survivors and caregivers found widespread awareness of colonoscopy as a CRC screening method but general lack of understanding of other test options despite some name recognition of Cologuard. Participants indicated that CRC screening information primarily came from physicians, who play a key role in educating and recommending, even urging, CRC screening. However, not all physicians recommend screening nor do they present alternatives to colonoscopy to all patients. Several participants noted that discussion of stool-based tests only occurred when colonoscopy was resisted. Having a personal connection with CRC (family history, knowing someone who died from CRC) increased general awareness but did not always seem to translate into knowing or meeting screening recommendations. Although not specifically mentioned by participants, their comments about perceptions and barriers to screening indicate that information is also passed within the community by jokes and comments about the colonoscopy preparation and procedure, and that this type of negative information is the most difficult to overcome.
Our results are similar to previous studies about CRC screening which found that financial burdens including cost and insurance coverage [9], fear and embarrassment, lack of perceived need (low perceived risk), and lack of provider recommendation hinder CRC screening [10]. We also found that specific qualities of the screening measures were important [10]. Unlike prior studies, we did not identify fear of diagnosis [9], fear of burdening family [9], health care delivery system or logistical issues [10], or cultural beliefs [10].
Provider recommendations are a crucial factor to increase CRC screening. Based on our results, participants lacked knowledge of fecal tests and they relied on PCP screening recommendations. Stool-based test are easy to perform, low cost, and non-invasive compared to colonoscopy, which address some barriers to CRC screening. Some patients prefer fecal tests versus a colonoscopy [16]. Therefore, providers ought to discuss all screening options with patients to promote shared decision-making based on patients’ needs, resources, frequency of testing, and preferences.
Our study participants suggested measures to improve CRC screening such as clinic-based education campaigns in restrooms, clinics, or waiting areas, use of church groups to increase awareness, and mass media (radio, billboards) targeted to the age group. Prior studies suggested one-to-one or group educational interventions, reminders, mass communication approaches, and provider-patient communication [17, 18].
Need for Theoretical Underpinning for Interventions
Our study indicated that increased general awareness of CRC did not translate into knowledge about risk, screening guidelines, or even screening behavior. Screening behavior is complex and involves individual, interpersonal, and systems-level factors. As such, interventions to promote CRC screening should be theoretically grounded. Systematic reviews focused on cancer screening interventions include an examination of constructs related to informed decision-making [19] and focused specifically on the use of Health Belief Model constructs for CRC screening [20]. Another systematic review of CRC interventions examined specific intervention components but did not report the underlying theoretical frameworks [21]. The literature on breast cancer screening is well-developed and includes many theoretically grounded intervention studies which would be informative for CRC screening programs. A scoping review conducted on rural breast cancer screening [22] identified the following theoretical frameworks being used: social learning theory, PRECEDE-PROCEED, Transtheoretical Model, communication-behavioral change model, and community organizational model.
Intersectionality of Rurality and Minority Status
Our focus groups highlighted the need for additional support of minority populations in rural communities. Rates of CRC are greater in rural vs. urban communities [4], but less is known about the intersectionality of rurality and minority status [23]. In their review study, Zahnd and colleagues discussed the need to focus increased efforts to understand and address the cancer disparities experienced by racial/ethnic minority populations living in rural communities [23]. They recommended research that examines how best to deliver the evidence-based practices to reduce health disparities in these populations, and we concur with their recommendations.
Strengths and Limitations
Strengths of our study include representation of multiple types of cancer and participants from multiple cancer centers serving areas of rural Nebraska. However, despite working with a cancer center in the western panhandle, we were not able to recruit participants from the sparsely populated frontier areas of the state. Of Nebraska’s 93 counties, 48 are classified as rural and 31 as frontier (< 7 residents per square mile) [24]; 62 counties are state-designated shortage areas for family practice [25], which is determined mainly by the population-to-physician ratio. These are areas where structural barriers such as travel, cost, and provider availability may be greater. Additionally, we did not specifically ask participants to report their CRC screening history.
Conclusions
Participant awareness of and knowledge about CRC screening methods varied across focus groups. Colonoscopy was the most widely known test but was associated with negative perceptions regarding the time, cost, and discomfort of the preparation and procedure. Promotion of CRC screening should include education about alternative test types, and informed decision-making between provider and patient regarding preferred screening methods based on the pros and cons of each test type. Individuals with a family history of colon issues (Crohn’s disease, CRC) are considered high-risk and need to be aware that screening should be discussed at earlier ages.
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Acknowledgements
Study data were collected and managed using REDCap electronic data capture tools hosted at UNMC. REDCap (Research Electronic Data Capture) is a secure, web-based application designed to support data capture for research studies. REDCap at UNMC is supported by Research IT Office funded by Vice Chancellor for Research (VCR). This publication’s contents are the sole responsibility of the authors and do not necessarily represent the official views of the VCR and NIH. We would like to thank our community partners who helped make this work possible, including Jolene Rohde, Comprehensive Cancer Control Program Manager at the Nebraska Department of Health and Human Services; Robert “Max” Norvell and Jenny Roush of CHI Health Regional Cancer Center, St. Francis; David Jones of Morrison Cancer Center, Mary Lanning Healthcare; and Tammy Neimoth of Great Plains Health Callahan Cancer Center. We would also like to thank the cancer survivors and caregivers who volunteered to participate in this research.
Funding
The cancer needs assessment was funded by the UNMC Fred & Pamela Buffett Cancer Center and its National Cancer Institute Cancer Center Support Grant (P30 CA036727).
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Study conceptualization and design (Kendra L. Ratnapradipa, Jordan Ranta, Tamara Robinson, Shinobu Watanabe-Galloway); data collection and analysis (Kendra L. Ratnapradipa, Krishtee Napit, Jordan Ranta, Lady Beverly Luma, Shinobu Watanabe-Galloway); data interpretation (all authors); writing—original draft (Kendra L. Ratnapradipa, Krishtee Napit, Jordan Ranta, Danae Dinkel, Shinobu Watanabe-Galloway); writing—review and editing (all authors); supervision (Kendra L. Ratnapradipa, Shinobu Watanabe-Galloway); final approval of manuscript (all authors).
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This was a focus group study conducted as part of an institutional needs assessment. The UNMC Institutional Review Board deemed this study as non-human subjects research.
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Ratnapradipa, K.L., Napit, K., Ranta, J. et al. Qualitative Analysis of Colorectal Cancer Screening in Rural Nebraska. J Canc Educ 38, 652–663 (2023). https://doi.org/10.1007/s13187-022-02170-y
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DOI: https://doi.org/10.1007/s13187-022-02170-y